Concentration dependence of vitamin C in combinations with vitamin e and zeaxanthin on light-induced toxicity to retinal pigment epithelial cells

Photochemistry and Photobiology

Volumn 88, Issue 6, 2012, Pages 1408-1417

  Rózanowska, Małgorzata ^a   Bakker, Linda ^a   Boulton, Michael E ^b   Rózanowski, Bartosz ^c  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF FLORIDA   (United States)

^c PEDAGOGICAL UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID;

CELL LINE; CELL SURVIVAL; CYTOLOGY; EPITHELIUM CELL; HUMAN; LIGHT; PHYSIOLOGY; PIGMENT EPITHELIUM; RADIATION RESPONSE;

ALPHA-TOCOPHEROL; ASCORBIC ACID; CELL LINE; CELL SURVIVAL; EPITHELIAL CELLS; HUMANS; LIGHT; RETINAL PIGMENT EPITHELIUM; VITAMIN E;

EID: 84868147519     PISSN: 00318655     EISSN: 17511097     Source Type: Journal    
DOI: 10.1111/j.1751-1097.2012.01228.x     Document Type: Article

References (66)

1. RóÅanowska, M., B. RóÅanowski, and, M. Boulton, (2009) Photobiology of the retina: Light damage to the retina. In Photobiological Sciences Online (Edited by, K. C. Smith,). American Society for Photobiology. Available at: http://www.photobiology.info. Accessed on 3 March 2012.
2. RóÅanowska, M., and, B. RóÅanowski, (2010) Uptake and photoprotection in cultured RPE cells. In Carotenoids: Physical, Chemical, and Biological Functions and Properties (Edited by, J. T. Landrum,), pp. 309-364. CRC Press, Boca Raton, FL.
3. Strauss, O., (2005) The retinal pigment epithelium in visual function. Physiol. Rev. 85, 845-881. (Pubitemid 40885218)
4. Buettner, G. R., (1993) The pecking order of free radicals and antioxidants: Lipid peroxidation, alpha-tocopherol, and ascorbate. Arch. Biochem. Biophys. 300, 535-543. (Pubitemid 23232908)
5. Edge, R., D. J. McGarvey, and, T. G. Truscott, (1997) The carotenoids as anti-oxidants-A review. J. Photochem. Photobiol., B 41, 189-200.
6. Bohm, F., R. Edge, D. J. McGarvey, and, T. G. Truscott, (1998) Beta-carotene with vitamins E and C offers synergistic cell protection against NOx. FEBS Lett. 436, 387-389. (Pubitemid 28482967)
7. Bohm, F., R. Edge, S. Foley, L. Lange, and, T. G. Truscott, (2001) Antioxidant inhibition of porphyrin-induced cellular phototoxicity. J. Photochem. Photobiol., B 65, 177-183. (Pubitemid 34110735)
8. Bohm, F., R. Edge, L. Lange, and, T. G. Truscott, (1998) Enhanced protection of human cells against ultraviolet light by antioxidant combinations involving dietary carotenoids. J. Photochem. Photobiol., B 44, 211-215. (Pubitemid 28466438)
9. Wrona, M., W. Korytowski, M. Rozanowska, T. Sarna, and, T. G. Truscott, (2003) Cooperation of antioxidants in protection against photosensitized oxidation. Free Radic. Biol. Med. 35, 1319-1329. (Pubitemid 37357257)
10. Wrona, M., M. Rozanowska, and, T. Sarna, (2004) Zeaxanthin in combination with ascorbic acid or alpha-tocopherol protects ARPE-19 cells against photosensitized peroxidation of lipids. Free Radic. Biol. Med. 36, 1094-1101. (Pubitemid 38479863)
11. El-Agamey, A., G. M. Lowe, D. J. McGarvey, A. Mortensen, D. M. Phillip, T. G. Truscott, and, A. J. Young, (2004) Carotenoid radical chemistry and antioxidant/pro-oxidant properties. Arch. Biochem. Biophys. 430, 37-48. (Pubitemid 39119778)
12. Sanz, M. M., L. E. Johnson, S. Ahuja, P. A. Ekstrom, J. Romero, and, T. van Veen, (2007) Significant photoreceptor rescue by treatment with a combination of antioxidants in an animal model for retinal degeneration. Neuroscience 145, 1120-1129. (Pubitemid 46463933)
13. Yin, J., F. Thomas, J. C. Lang, and, E. Chaum, (2011) Modulation of oxidative stress responses in the human retinal pigment epithelium following treatment with vitamin C. J. Cell. Physiol. 226, 2025-2032.
14. Traber, M. G., and, J. F. Stevens, (2011) Vitamins C and E: Beneficial effects from a mechanistic perspective. Free Radic. Biol. Med. 51, 1000-1013.
15. Biesalski, H. K., and, J. Tinz, (2008) Nutritargeting. Adv. Food Nutr. Res. 54, 179-217.
16. Rice, M. E., and, I. Russo-Menna, (1998) Differential compartmentalization of brain ascorbate and glutathione between neurons and glia. Neuroscience 82, 1213-1223. (Pubitemid 27502062)
17. Kramarenko, G. G., S. G. Hummel, S. M. Martin, and, G. R. Buettner, (2006) Ascorbate reacts with singlet oxygen to produce hydrogen peroxide. Photochem. Photobiol. 82, 1634-1637. (Pubitemid 46158856)
18. Buettner, G. R., T. P. Doherty, and, T. D. Bannister, (1984) Hydrogen peroxide and hydroxyl radical formation by methylene blue in the presence of ascorbic acid. Radiat. Environ. Biophys. 23, 235-243. (Pubitemid 14001642)
19. Kramarenko, G. G., W. W. Wilke, D. Dayal, G. R. Buettner, and, F. Q. Schafer, (2006) Ascorbate enhances the toxicity of the photodynamic action of Verteporfin in HL-60 cells. Free Radic. Biol. Med. 40, 1615-1627. (Pubitemid 44316662)
20. Buettner, G. R., and, M. J. Need, (1985) Hydrogen peroxide and hydroxyl free radical production by hematoporphyrin derivative, ascorbate and light. Cancer Lett. 25, 297-304. (Pubitemid 15171771)
21. Kelley, E. E., F. E. Domann, G. R. Buettner, L. W. Oberley, and, C. P. Burns, (1997) Increased efficacy of in vitro Photofrin photosensitization of human oral squamous cell carcinoma by iron and ascorbate. J. Photochem. Photobiol., B 40, 273-277. (Pubitemid 27478313)
22. Rozanowska, M., A. Bober, J. M. Burke, and, T. Sarna, (1997) The role of retinal pigment epithelium melanin in photoinduced oxidation of ascorbate. Photochem. Photobiol. 65, 472-479. (Pubitemid 27158986)
23. Rozanowska, M., W. Korytowski, B. Rozanowski, C. Skumatz, M. E. Boulton, J. M. Burke, and, T. Sarna, (2002) Photoreactivity of aged human RPE melanosomes: A comparison with lipofuscin. Invest. Ophthalmol. Vis. Sci. 43, 2088-2096. (Pubitemid 34700632)
24. Rozanowski, B., J. Burke, T. Sarna, and, M. Rozanowska, (2008) The pro-oxidant effects of interactions of ascorbate with photoexcited melanin fade away with aging of the retina. Photochem. Photobiol. 84, 658-670. (Pubitemid 351589368)
25. Rozanowski, B., J. M. Burke, M. E. Boulton, T. Sarna, and, M. Rozanowska, (2008) Human RPE melanosomes protect from photosensitized and iron-mediated oxidation but become pro-oxidant in the presence of iron upon photodegradation. Invest. Ophthalmol. Vis. Sci. 49, 2838-2847.
26. He, X., P. Hahn, J. Iacovelli, R. Wong, C. King, R. Bhisitkul, M. Massaro-Giordano, and, J. L. Dunaief, (2007) Iron homeostasis and toxicity in retinal degeneration. Prog. Retin. Eye Res. 26, 649-673. (Pubitemid 47615564)
27. Dunaief, J. L., (2006) Iron induced oxidative damage as a potential factor in age-related macular degeneration: The Cogan Lecture. Invest. Ophthalmol. Vis. Sci. 47, 4660-4664. (Pubitemid 46586359)
28. Dentchev, T., P. Hahn, and, J. L. Dunaief, (2005) Strong labeling for iron and the iron-handling proteins ferritin and ferroportin in the photoreceptor layer in age-related macular degeneration. Arch. Ophthalmol. 123, 1745-1746. (Pubitemid 41785113)
29. Hahn, P., A. H. Milam, and, J. L. Dunaief, (2003) Maculas affected by age-related macular degeneration contain increased chelatable iron in the retinal pigment epithelium and Bruch's membrane. Arch. Ophthalmol. 121, 1099-1105. (Pubitemid 36962162)
30. Hahn, P., G. S. Ying, J. Beard, and, J. L. Dunaief, (2006) Iron levels in human retina: Sex difference and increase with age. NeuroReport 17, 1803-1806. (Pubitemid 44948111)
31. Resnikoff, S., D. Pascolini, D. Etya'ale, I. Kocur, R. Pararajasegaram, G. P. Pokharel, and, S. P. Mariotti, (2004) Global data on visual impairment in the year 2002. Bull. World Health Organ. 82, 844-851. (Pubitemid 39573742)
32. Augood, C. A., J. R. Vingerling, P. T. de Jong, U. Chakravarthy, J. Seland, G. Soubrane, L. Tomazzoli, F. Topouzis, G. Bentham, M. Rahu, J. Vioque, I. S. Young, and, A. E. Fletcher, (2006) Prevalence of age-related maculopathy in older Europeans: The European Eye Study (EUREYE). Arch. Ophthalmol. 124, 529-535.
33. World Health Organization. (2008) The Global Burden of Disease: 2004 Update. World Health Organization, Geneva, Switzerland.
34. Jarrett, S. G., J. Albon, and, M. Boulton, (2006) The contribution of DNA repair and antioxidants in determining cell type-specific resistance to oxidative stress. Free Radic. Res. 40, 1155-1165. (Pubitemid 44490156)
35. Zareba, M., M. W. Raciti, M. M. Henry, T. Sarna, and, J. M. Burke, (2006) Oxidative stress in ARPE-19 cultures: Do melanosomes confer cytoprotection? Free Radic. Biol. Med. 40, 87-100. (Pubitemid 41759406)
36. Alvarez, R. A., G. I. Liou, S. L. Fong, and, C. D. Bridges, (1987) Levels of alpha- and gamma-tocopherol in human eyes: Evaluation of the possible role of IRBP in intraocular alpha-tocopherol transport. Am. J. Clin. Nutr. 46, 481-487. (Pubitemid 18003386)
37. Redmond, R. W., and, J. N. Gamlin, (1999) A compilation of singlet oxygen yields from biologically relevant molecules. Photochem. Photobiol. 70, 391-475. (Pubitemid 129555813)
38. Rozanowska, M., K. Handzel, M. E. Boulton, and, B. Rozanowski, (2012) Cytotoxicity of all-trans-retinal increases upon photodegradation. Photochem. Photobiol. (In press, DOI: 10.1111/j.1751-1097.2012.01161.x)
39. Mosmann, T., (1983) Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63. (Pubitemid 14203433)
40. Rozanowski, B., J. Cuenco, S. Davies, F. A. Shamsi, A. Zadlo, P. Dayhaw-Barker, M. Rozanowska, T. Sarna, and, M. E. Boulton, (2008) The phototoxicity of aged human retinal melanosomes. Photochem. Photobiol. 84, 650-657. (Pubitemid 351589361)
41. Allen, M. T., M. Lynch, A. Lagos, R. W. Redmond, and, I. E. Kochevar, (1991) A wavelength dependent mechanism for rose bengal-sensitized photoinhibition of red cell acetylcholinesterase. Biochim. Biophys. Acta 1075, 42-49.
42. Kochevar, I. E., C. R. Lambert, M. C. Lynch, and, A. C. Tedesco, (1996) Comparison of photosensitized plasma membrane damage caused by singlet oxygen and free radicals. Biochim. Biophys. Acta 1280, 223-230. (Pubitemid 26164039)
43. Lambert, C. R., H. Stiel, D. Leupold, M. C. Lynch, and, I. E. Kochevar, (1996) Intensity-dependent enzyme photosensitization using 532 nm nanosecond laser pulses. Photochem. Photobiol. 63, 154-160. (Pubitemid 126478005)
44. Lambert, C. R., and, I. E. Kochevar, (1997) Electron transfer quenching of the rose bengal triplet state. Photochem. Photobiol. 66, 15-25. (Pubitemid 127470628)
45. Zhuang, S., M. C. Lynch, and, I. E. Kochevar, (1999) Caspase-8 mediates caspase-3 activation and cytochrome c release during singlet oxygen-induced apoptosis of HL-60 cells. Exp. Cell Res. 250, 203-212. (Pubitemid 29391584)
46. Kochevar, I. E., J. Bouvier, M. Lynch, and, C. W. Lin, (1994) Influence of dye and protein location on photosensitization of the plasma membrane. Biochim. Biophys. Acta 1196, 172-180.
47. Kato, H., K. Komagoe, Y. Nakanishi, T. Inoue, and, T. Katsu, (2012) Xanthene dyes induce membrane permeabilization of bacteria and erythrocytes by photoinactivation. Photochem. Photobiol. 88, 423-431.
48. Killig, F., G. Stark, and, H. J. Apell, (2004) Photodynamic inactivation of the Na, K-ATPase occurs via different pathways. J. Membr. Biol. 200, 133-144. (Pubitemid 39426113)
49. Yang, P., M. Yao, S. L. Demartelaere, R. W. Redmond, and, I. E. Kochevar, (2012) Light-activated sutureless closure of wounds in thin skin. Lasers Surg. Med. 44, 163-167.
50. Wang, Y., I. E. Kochevar, R. W. Redmond, and, M. Yao, (2011) A light-activated method for repair of corneal surface defects. Lasers Surg. Med. 43, 481-489.
51. Verter, E. E., T. E. Gisel, P. Yang, A. J. Johnson, R. W. Redmond, and, I. E. Kochevar, (2011) Light-initiated bonding of amniotic membrane to cornea. Invest. Ophthalmol. Vis. Sci. 52, 9470-9477.
52. Tsao, S., M. Yao, H. Tsao, F. P. Henry, Y. Zhao, J. J. Kochevar, R. W. Redmond, and, I. E. Kochevar, (2012) Light-activated tissue bonding for excisional wound closure: A split-lesion clinical trial. Br. J. Dermatol. 166, 555-563.
53. Gu, C., T. Ni, E. E. Verter, R. W. Redmond, I. E. Kochevar, and, M. Yao, (2011) Photochemical tissue bonding: A potential strategy for treating limbal stem cell deficiency. Lasers Surg. Med. 43, 433-442.
54. Franco, R. A., J. R. Dowdall, K. Bujold, C. Amann, W. Faquin, R. W. Redmond, and, I. E. Kochevar, (2011) Photochemical repair of vocal fold microflap defects. Laryngoscope 121, 1244-1251.
55. Rozanowska, M., and, T. Sarna, (2005) Light-induced damage to the retina: Role of rhodopsin chromophore revisited. Photochem. Photobiol. 81, 1305-1330. (Pubitemid 43035839)
56. Sliney, D. H., (2005) Exposure geometry and spectral environment determine photobiological effects on the human eye. Photochem. Photobiol. 81, 483-489. (Pubitemid 40901315)
57. Rozanowska, M., A. Pawlak, B. Rozanowski, C. Skumatz, M. Zareba, M. E. Boulton, J. M. Burke, T. Sarna, and, J. D. Simon, (2004) Age-related changes in the photoreactivity of retinal lipofuscin granules: Role of chloroform-insoluble components. Invest. Ophthalmol. Vis. Sci. 45, 1052-1060. (Pubitemid 38869007)
58. Rozanowska, M., J. Ciszewska, W. Korytowski, and, T. Sarna, (1995) Rose-bengal-photosensitized formation of hydrogen peroxide and hydroxyl radicals. J. Photochem. Photobiol. B: Biol. 29, 71-77.
59. Halliwell, B., and, J. M. C. Gutteridge, (1998) Free Radicals in Biology and Medicine. Oxford University Press, New York.
60. Corti, A., A. F. Casini, and, A. Pompella, (2012) Cellular pathways for transport and efflux of ascorbate and dehydroascorbate. Arch. Biochem. Biophys. 500, 107-115.
61. Sakurai, K., A. Nabeyama, and, Y. Fujimoto, (2006) Ascorbate-mediated iron release from ferritin in the presence of alloxan. Biometals 19, 323-333. (Pubitemid 43946172)
62. Levine, M., S. J. Padayatty, and, M. G. Espey, (2011) Vitamin C: A concentration-function approach yields pharmacology and therapeutic discoveries. Adv. Nutr. 2, 78-88.
63. Fiedor, J., L. Fiedor, R. Haessner, and, H. Scheer, (2005) Cyclic endoperoxides of beta-carotene, potential pro-oxidants, as products of chemical quenching of singlet oxygen. Biochim. Biophys. Acta 1709, 1-4. (Pubitemid 41096087)
64. Stoyanovsky, D. A., R. Goldman, R. M. Darrow, D. T. Organisciak, and, V. E. Kagan, (1995) Endogenous ascorbate regenerates vitamin E in the retina directly and in combination with exogenous dihydrolipoic acid. Curr. Eye Res. 14, 181-189.
65. Dunn, K. C., A. E. Aotaki-Keen, F. R. Putkey, and, L. M. Hjelmeland, (1996) ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp. Eye Res. 62, 155-169. (Pubitemid 26140102)
66. Age-Related Eye Disease Study Group. (2001) A randomized, placebo-controlled, clinical trial of high-dose supplementation with vitamins C and E and beta carotene for age-related cataract and vision loss: AREDS report no. 9. Arch. Ophthalmol. 119, 1439-1452.